Bifurcation and Enhancement of Autonomous-Nonautonomous Retrotransposon Partnership through LTR Swapping in Soybean

Abstract

Long terminal repeat (LTR) retrotransposons, the most abundant genomic components in flowering plants, are classifiable into autonomous and nonautonomous elements based on their structural completeness and transposition capacity. It has been proposed that selection is the major force for maintaining sequence (e.g., LTR) conservation between nonautonomous elements and their autonomous counterparts. Here, we report the structural, evolutionary, and expression characterization of a giant retrovirus-like soybean (Glycine max) LTR retrotransposon family, SNARE. This family contains two autonomous subfamilies, SARE(A) and SARE(B), that appear to have evolved independently since the soybean genome tetraploidization event approximately 13 million years ago, and a nonautonomous subfamily, SNRE, that originated from SARE(A). Unexpectedly, a subset of the SNRE elements, which amplified from a single founding SNRE element within the last approximately 3 million years, have been dramatically homogenized with either SARE(A) or SARE(B) primarily in the LTR regions and bifurcated into distinct subgroups corresponding to the two autonomous subfamilies. We uncovered evidence of region-specific swapping of nonautonomous elements with autonomous elements that primarily generated various nonautonomous recombinants with LTR sequences from autonomous elements of different evolutionary lineages, thus revealing a molecular mechanism for the enhancement of preexisting partnership and the establishment of new partnership between autonomous and nonautonomous elements.